Cited by 296Neuroinflammation and Neurodegeneration MechanismsStress Responses and CortisolTryptophan and brain disorders

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Stress-Induced Neuronal Colony Stimulating Factor 1 Provokes Microglia-Mediated Neuronal Remodeling and Depressive-like Behavior

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Wohleb, Eric S., Terwilliger, Rosemarie, Duman, Catharine H., Duman, Ronald S.·2018·Biological Psychiatry

DOI 10.1016/j.biopsych.2017.05.026PMC PMC6506225

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Abstract

Background Chronic stress exposure causes neuronal atrophy and synaptic deficits in the medial prefrontal cortex (PFC), contributing to development of anxiety- and depressive-like behaviors. Concomitantly, microglia in the PFC undergo morphological and functional changes following stress exposure, suggesting that microglia contribute to synaptic deficits underlying behavioral consequences.Methods Male and female mice were exposed to chronic unpredictable stress (CUS) to examine the role of neuron-microglia interactions in the medial PFC during development of anxiety- and depressive-like behaviors. Thy1-GFP-M mice were used to assess microglia-mediated neuronal remodeling and dendritic spine density in the medial PFC. Viral-mediated knockdown of neuronal colony stimulating factor 1 (CSF1) was used to modulate microglia function and behavioral consequences after CUS.Results CUS promoted anxiety- and depressive-like behaviors that were associated with increased messenger RNA levels of CSF1 in the PFC. Increased CSF1 messenger RNA levels were also detected in the postmortem dorsolateral PFC of individuals with depression. Moreover, microglia isolated from the frontal cortex of mice exposed to CUS show elevated CSF1 receptor expression and increased phagocytosis of neuronal elements. Notably, functional alterations in microglia were more pronounced in male mice compared with female mice. These functional changes in microglia corresponded with reduced dendritic spine density on pyramidal neurons in layer 1 of the medial PFC. Viral-mediated knockdown of neuronal CSF1 in the medial PFC attenuated microglia-mediated neuronal remodeling and prevented behavioral deficits caused by CUS.Conclusions These findings revealed that stress-induced elevations in neuronal CSF1 provokes microglia-mediated neuronal remodeling in the medial PFC, contributing to synaptic deficits and development of anxiety- and depressive-like behavior.

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Authors: Wohleb, E. S., Terwilliger, R., Duman, C. H., & Duman, R. S.
Affiliations: Yale University (US)
Corresponding author: Wohleb, Eric S.
ORCID: Wohleb, Eric S.
Duman, Catharine H.
Duman, Ronald S.
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 2018-01
Volume: 83
Issue: 1
Pages: 38-49
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/j.biopsych.2017.05.026
PMC: PMC6506225
OpenAlex: W2730743637
Cited by: 288
References: 67
Citations by year: 2026: 23 · 2025: 39 · 2024: 31 · 2023: 34 · 2022: 37 · 2021: 49 · 2020: 28 · 2019: 30 · 2018: 14
FWCI: 9.74
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Biological Psychiatry (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (R01MH093897, R37MH045481, R01MH045481)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Keywords: chronic unpredictable mild stress, colony-stimulating factor 1, microglia, neuronal remodeling, medial prefrontal cortex, depression-like behavior, anxiety-like behavior, dendritic spine density, synaptic deficits, CSF-1 receptor, microglial phagocytosis, sex differences, depression
MeSH terms: Animals, Anxiety, Chronic Disease, Depressive Disorder, Disease Models, Animal, Female, Male, Mice, Inbred C57BL, Mice, Transgenic, Neuronal Plasticity, Neurons, Phagocytosis, RNA, Messenger, Sex Characteristics, Stress, Psychological, Macrophage Colony-Stimulating Factor, Receptor, Macrophage Colony-Stimulating Factor, Prefrontal Cortex, Microglia, Uncertainty

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Stress-Induced Neuronal Colony Stimulating Factor 1 Provokes Microglia-Mediated Neuronal Remodeling and Depressive-like Behavior

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